Relationship between repetitive firing and afterhyperpolarizations in human neocortical neurons
Abstract
1. Human neocortical neurons fire repetitively in response to long depolarizing current injections. The slope of the relationship between average firing frequency and injected current (f-I slope) was linear or bilinear in these cells. The mean steady-state f-I slope (average of the last 500 ms of a 1-s firing episode) was 57.8 Hz/nA. The instantaneous firing rate decreased with time during a 1-s constant-current injection (spike frequency adaptation). Also, human neurons exhibited habituation in response to a 1-s current stimulus repeated every 2 s. 2. Afterhyperpolarizations (AHPs) reflect the active ionic conductances after action potentials. We studied AHPs with the use of intracellular recordings and pharmacological manipulations in the in vitro slice preparation to 1) gain insight into the ionic mechanisms underlying the AHPs and 2) elucidate the role that the underlying currents play in the functional behavior of human cortical neurons. 3. We have classified three AHPs in human neocortical neurons on the basis of their time courses: fast, medium, and slow. The amplitude of the AHPs was dependent on stimulus intensity and duration, number and frequency of spikes, and membrane potential. 4. The fast AHP had a reversal potential of -65 mV and was eliminated in extracellular Co2+, tetraethylammonium (TEA) or 4-aminopyridine, and intracellular TEA or CsCl. These manipulations also caused an increase in spike width. 5. The medium AHP had a reversal potential of -90 to -93 mV (22-24 mV hyperpolarized from mean resting potential). This AHP was reduced by Co2+, apamin, tubocurare, muscarine, norepinephrine (NE), and serotonin (5-HT). Pharmacological manipulations suggest that the medium AHP is produced in part by 1) a Ca-dependent K+ current and 2) a time-dependent anomalous rectifier (IH). 6. The slow AHP reversed at -83 to -87 mV (14-18 mV hyperpolarized from mean resting potential). This AHP was diminished by Co2+, muscarine, NE, and 5-HT. The pharmacology of the slow AHP suggests that a Ca-dependent K+ current with slow kinetics contributes to this AHP. 7. The currents involved in the fast AHP are important in spike repolarization, control of interspike interval during repetitive firing, and prevention of burst firing. Currents underlying the medium and slow AHPs influence the interspike interval during repetitive firing and produce spike frequency adaptation and habituation.
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Activation of mAChRs on cortical pyramidal neurons increases excitability via Ca2+-dependent potassium channels.
“increases excitability via Ca2+-dependent potassium channels177–179”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [177]
AHP currents are mainly mediated by calcium-dependent potassium channels, but also partly by calcium-independent potassium channels.
“AHP currents are mainly mediated by calcium-dependent potassium channels [77, 78], but also partly by calcium-independent potassium channels [79].”
From Chronic unpredictable stress induces depression-related behaviors by suppressing AgRP neuron activity (2021) · cites this paper as [79]
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“Both the mAHP and the sAHP are Ca 2ϩ -dependent (Connors et al. 1984; Lorenzon and Foehring 1992, 1993; Pineda et al. 1998; Schwindt et al. 1988b) and increase in amplitude with number and frequency of spikes (as do increases in [Ca 2ϩ ] i ).”
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“…sAHP channels. sAHP rise phase kinetics At physiological temperatures, the sAHP (and the underlying IsAHP) reaches its peak slowly ( 122 ms for IsAHP) and decays much slower than the mAHP ( 1–2 s for both the sAHP and IsAHP) (Lorenzon and Foehring 1992; Pineda et al. 1998; Schwindt et al. 1988a,b).”
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“We also showed that AP repolarization in mouse layer 2/3, etv1, or glt cells is not Ca2 dependent (Guan et al. 2015), consistent with previous studies on neocortical pyramidal cells (Lorenzon and Foehring 1992; Pineda et al. 1999; Schwindt et al. 1988a, 1988b).”
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“Reduced conductance of the delayed rectifier caused a concurrent reduction in the AHP, in line with previous work (Lorenzon and Foehring, 1992).”
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“If spike frequency adaptation in SGNs is Ca 2 dependent via IKCa, as has been documented in other systems (Lorenzon and Foehring, 1992; Kim and Rieke, 2001; Groth et al., 2011), it would be consistent with the finding that apical neurons express larger Ca 2 current magnitude than basal neurons.”
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“It diminishes, through activation of muscarinic M1 receptors of pyramidal cells, a Ca2+ dependent K+ current, which leads to depolarisation and hence directly increases cellular excitability (McCormick and Prince 1986; Schwindt et al. 1988; Lorenzon and Foehring 1992).”
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“Results indicate that application of ACh and muscarinic agonists reduces or entirely abolishes the sAHP in a variety of tissue types and species (Schwindt et al., 1988b; McCormick and Williamson, 1989; Lorenzon and Foehring, 1992; Muller et al., 1992; Pedarzani and Storm, 1996; Klink and Alonso, 1997).”
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“A larger spike increases the amplitude of the hyperpolarization, which in turn increases the subsequent spike [265].”
BackgroundRaes, A. L., Wang, Z., van den Berg, R. J., Goethals, M., de Vijver, G. V., & Bogaert, P. P. V. (1997) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240050434 · Cited by 20 · see citing works
Human in vitro systems for examining synaptic function and plasticity in the brain
Lee, K., Park, T., Heppner, P. A., Schweder, P. M., Mee, E. W., Dragunow, M., & Montgomery, J. M. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00411.2019 · Cited by 20 · see citing works
Lavigne, F., Dumercy, L., & Darmon, N. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21504 · Cited by 20 · see citing works
“SFA has been observed in many types of neurons and in many species (see Puccini et al., 2006; Fuhrmann, Markram, & Tsodyks, 2002), including human neocortical cells (Lorenzon & Foehring, 1992; Foehring, Lorenzon, Herron, & Wilson, 1991; Avoli & Olivier, 1989).”
BackgroundThe clinical and prognostic relevance of the postictal slow focus in the electrocorticogram
Hufnagel, A., Poersch, M., Elger, C. E., et al. (1995) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(94)00229-e · Cited by 20 · see citing works
Newkirk, G. S., Guan, D., Dembrow, N. C., Armstrong, W. E., Foehring, R. C., & Spain, W. J. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab266 · Cited by 19 · see citing works
Self-citationFord, K., Arroyo, D. A., Kay, J. N., Lloyd, E. E., Bryan, R. M., Sanes, J. R., & Feller, M. B. (2013) · Journal of Neurophysiology · doi:10.1152/jn.01085.2012 · Cited by 19 · see citing works
Vatanparast, J., & Janahmadi, M. (2008) · Brain Research · doi:10.1016/j.brainres.2008.12.003 · Cited by 19 · see citing works
Khawaja, F. A., Alonso, A. A., & Bourque, C. W. (2007) · Hippocampus · doi:10.1002/hipo.20365 · Cited by 18 · see citing works
Lorenzon, N. M., & Foehring, R. C. (1995) · Developmental Brain Research · doi:10.1016/0165-3806(94)00171-u · Cited by 18 · see citing works
Self-citationPsarrou, M., Stefanou, S. S., Papoutsi, A., Tzilivaki, A., Vassilis Cutsuridis, A., & Poirazi, P. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00287 · Cited by 18 · see citing works
“Both fast and slow AHP currents were present in the soma and much less in the apical dendrites (Lorenzon and Foehring, 1992).”
BackgroundMethodParadoxical Excitatory Impact of SK Channels on Dendritic Excitability
Bock, T., Honnuraiah, S., & Stuart, G. J. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0105-19.2019 · Cited by 17 · see citing works
“Although the inhibitory impact of somatic SK channels on neuronal excitability is well established (Schwindt et al., 1988a, 1992; Lorenzon and Foehring, 1992; Hirschberg et al., 1999; Jones and Stuart, 2013), what underlies the excitatory impact of dendritic SK channels?”
BackgroundStrauß, U., Zhou, F., Henning, J., Battefeld, A., Wree, A., Köhling, R., Haas, S. J.-P., Benecke, R., Rolfs, A., & Gimsa, U. (2008) · Journal of Neurophysiology · doi:10.1152/jn.00402.2007 · Cited by 17 · see citing works
Inhibition in the Cortical Network
Benardo, L. S., & Wong, R. K. S. (1995) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195083309.003.0010 · Cited by 17 · see citing works
(1995) · doi:10.1093/acprof:oso/9780195083309.001.0001 · Cited by 17 · see citing works
Callister, R. J., Laidlaw, D. H., & Stuart, D. G. (1995) · Journal of Morphology · doi:10.1002/jmor.1052250206 · Cited by 16 · see citing works
Overview: Basic Elements of the Cortical Network
Jones, E. G. (1995) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195083309.003.0008 · Cited by 16 · see citing works
Burrell, B. D., & Crisp, K. M. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00989.2007 · Cited by 16 · see citing works
Palma, J., Massimiliano Versace, A., & Grossberg, S. (2011) · Journal of Computational Neuroscience · doi:10.1007/s10827-011-0354-8 · Cited by 14 · see citing works
“…References fAHP Spike-based 0.8 −65 6.7 0.1 2.0 0.6 n/a Ca-based BK 0.9 −65 3.2 n/a n/a 0.8 n/a A 0.98 −80 Rat Hippocampus n/a −65 7 n/a 2–5 0.9 (Storm 1987) Human Neocortex n/a −65 n/a n/a n/a n/a (Lorenzon and Foehring 1992) Cat Sensorimotor n/a −71 10 n/a n/a n/a (Schwindt et al.…”
BackgroundMethodResultInfluentialGrossberg, S., Palma, J., & Massimiliano Versace, A. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00501 · Cited by 13 · see citing works
“The active category can therefore resonate with the attended features X∗ to drive new learning.”
BackgroundGisabella, B., Bolshakov, V. Y., & Benes, F. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032483 · Cited by 13 · see citing works
“The observed decreases in the spiking output of SO interneurons in the presence of KA in PICRO rats may, in part, be explained by the increased AHP’s between the spikes in the course of firing, resulting in spike frequency accommodation [24,25,26,27].”
Roychowdhury, S., Zwierzchowski-Zarate, A. N., García‐Oscos, F., Cuevas‐Olguin, R., Delgado, R. S., & Atzori, M. (2014) · Neurochemical Research · doi:10.1007/s11064-014-1440-x · Cited by 12 · see citing works
“This effect opposes the increase in intrinsic excitability of principal cells associated with decreased K conductances such as after hyperpolarization (AHP), induced by NE [4, 31], as well as by several other neuromodulators [32, 33].”
Bases fisiopatológicas de la epilepsia del lóbulo temporal: estudios en humanos y animales
Pastor, J., Uzcategui, Y. G., Gal, B., Rabbione, G. J. O., de Sola, R. G., & de la Prida, L. M. (2006) · Revista de Neurología · doi:10.33588/rn.4211.2006142 · Cited by 13 · see citing works
“En neuronas neocorticales humanas se han descrito conductancias de Na, K y Ca con características similares a las estudiadas en animales [79-85].”
BackgroundSynaptic Plasticity in Hippocampus and Neocortex: A Comparison
Malenka, R. C. (1995) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195083309.003.0007 · Cited by 11 · see citing works
- Authors
- Lorenzon, N. M., & Foehring, R. C.
- Affiliations
- Department of Anatomy and Neurobiology, University of Tennessee,Memphis 38103-4901.
- ORCID
- Foehring, R. C.
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 1992-02-01
- Volume
- 67
- Issue
- 2
- Pages
- 350-363
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W2399267155
- Cited by
- 145
- References
- 0
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 2 · 2022: 1 · 2021: 2 · 2020: 2 · 2019: 1 · 2018: 4 · 2017: 3 · 2016: 3 · 2015: 2 · 2014: 3 · 2013: 2 · 2012: 4
- FWCI
- 5.03
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r29ns027180-05)
- National Institute of Neurological Disorders and Stroke (R29 NS-27180)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- afterhyperpolarization, repetitive firing, spike frequency adaptation, calcium-activated potassium current, tetraethylammonium, apamin, muscarinic receptors, norepinephrine, serotonin, habituation, in vitro slice preparation, intracellular recording
- MeSH terms
- Action Potentials, Apamin, Cerebral Cortex, Cobalt, Electrophysiology, Epilepsy, Humans, Ion Channels, Membrane Potentials, Microelectrodes, Neural Conduction, Neurons, Serotonin, Tetraethylammonium Compounds, 4-Aminopyridine, In Vitro Techniques
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